Circadian timing in central and peripheral tissues in a migratory songbird: dependence on annual life-history states

FASEB J. 2015 Oct;29(10):4248-55. doi: 10.1096/fj.15-275339. Epub 2015 Jun 23.


Predictable seasonal change in photoperiod triggers a sequential change in the daily activity-rest pattern, adaptive for migration in several bird species. The night-migratory black-headed bunting (Emberiza melanocephala) is day active under short photoperiods (8 h light:16 h dark, short day sensitive). Under long photoperiods (16 h light:8 h dark), the buntings are initially day active (long day premigratory) but subsequently become intensely night active (long day migratory) and after few weeks again return to a day active pattern (long day refractory). However, it is unclear how the daily expression of circadian genes changes during photoperiod-induced seasonal life-history states (LHSs). We measured period 2 (Per2), cryptochrome 1 (Cry1), brain and muscle arnt-like protein 1 (Bmal1), and circadian locomotor output cycles kaput (Clock) mRNA expressions in various neural and peripheral tissues of buntings in different LHSs and discovered differences of ∼2 to 6 h in the phase and 2- to 4-fold in amplitude of circadian oscillations of Per2, Cry1, and Bmal1 between photoperiod-induced LHSs. Phase relationship in mRNA oscillations was altered between oscillator components in the circadian pacemaker system (retina, pineal, hypothalamus) as well as in the peripheral (liver, muscle) tissues. These results show for the first time altered waveforms of clock gene expressions in all tissues in parallel with behavioral shifts and suggest the involvement of circadian system in photoperiod induction of seasonal LHSs in a migratory species.

Keywords: Bmal1; Clock; black-headed bunting; circadian genes; cryptochrome.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • ARNTL Transcription Factors / genetics
  • Animal Migration / physiology*
  • Animals
  • Avian Proteins / genetics
  • CLOCK Proteins / genetics
  • Circadian Rhythm*
  • Cryptochromes / genetics
  • Gene Expression
  • Hypothalamus / metabolism
  • Liver / metabolism
  • Male
  • Muscles / metabolism
  • Period Circadian Proteins / genetics
  • Photoperiod*
  • Pineal Gland / metabolism
  • Retina / metabolism
  • Reverse Transcriptase Polymerase Chain Reaction
  • Seasons
  • Songbirds / genetics
  • Songbirds / physiology*


  • ARNTL Transcription Factors
  • Avian Proteins
  • Cryptochromes
  • Period Circadian Proteins
  • CLOCK Proteins